Journal of Asia-Pacific Entomology 21 (2018) 46–51

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Journal of Asia-Pacific Entomology

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Olfactory behavior and response of household () to MARK different types of coffee odor: A coffee-based bait development prospect ⁎ Abdul Hafiz Ab Majida, , Hamady Diengb, Siti Salbiah Elliasa, Faezah Syukriah Sabtua, Abd Hafis Abd Rahima, Tomomitsu Sathoc a Household and Structural Urban Entomology Laboratory, Vector Control Research Unit, School of Biological Sciences, Universiti Sains Malaysia, Malaysia b Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia c Department of Microbiology, Faculty of Pharmaceutical Sciences, Fukuoka University, 8-19-1 Nanakuma, Johan-ku, 814-0180 Fukuoka, Japan

ARTICLE INFO ABSTRACT

Keywords: Odor sensation is a sensory modality of considerable significance in the foraging behavior and interactional Household ants organization of ants. In the food bait technology, smell is the basis of attraction, which, in turn, is the line of bait Olfactory use and a key parameter for judging efficacy. Yet, the currently available baits possess low attractiveness to ff Co ee many pests. Hence, strategies to produce ant bait with increased attractiveness are needed. Despite evidence Behavioral effects that coffee has a diverse aroma complex that affects the behavior of honey bees and ants, its attraction to house- invading ants has yet to be investigated. In a series of Y-tube olfactometer bioassays, we examined the behavioral responses of indicum (TI), Monomorium pharaonis (MP) and Solenopsis geminata (SG) to various coffee- induced odor stimuli, comprised of extracts from Arabica, Robusta and Liberica. All coffee extracts showed an influence on the behavior of TI, MP and SG workers, with Arabica showed the most significant influence to the tested ants. The workers of TI, MP and SG were more attracted to the odor of 0.01% Arabica extract (ONE), in comparison with 0.05% Arabica extract (TWO) or 0.10% Arabica extract (THREE). Arabica extract mixed with sugar (S) elicited a significant attraction from workers of all three species in a balanced competition with either unsweetened Arabica extract or water. These results indicated that coffee, particularly Arabica, was attractive to the foragers of TI, MP and SG, thus, the use of coffee as a novel stimulus agent seems plausible in ant bait development.

Introduction Granovsky, 1990; Smith and Whitman, 1992) and may feed on wounds (Anon, 1986), thus, considered as a potential disease vector (Osae et al., There are > 12,000 known species of ants (Hammond, 2011), many 2011). S. geminata, on the other hand, is a major threat to agricultural of which are among the most common invading or living inside crops (Wilson, 2005), affecting farmers' performance by inflicting irri- human establishments where they become a nuisance and cause da- tating stings (Hill, 1987; Nestel and Dickschen, 1990). This type of ant mage (Lee, 2002). The typical house invaders are dolichoderine ants also causes substantial damage to PVC coatings of electrical wiring such as Tapinoma indicum (Lee, 2002; Man and Lee, 2014), Monomorium (Prins, 1985) and drip irrigation tubing (Chang and Ota, 1990). pharaonis (Osae et al., 2011) and Solenopsis geminata (Harris et al., Efforts to combat such damages rely heavily on the use of chemical 2005). insecticides through baiting (Higgins et al., 1997), residual perimeter Among the species, T. indicum is the most nuisance, having the sprays (Potter and Hillery, 2002), or both (Higgins et al., 1997). In ability to invade any disturbed habitats suitable for its nesting and these global strategies against ant pests, baiting forms a very crucial subsequently forms large-sized colonies (Passera, 1994). Another part of the solution (Jordan et al., 2013). This method takes advantage house-invading ant species, M. pharaonis (also known as the Pharaoh of the social trophallactic and grooming behaviors of ants (Lee, 2008) ants), attacks a wide range of foodstuffs, clothes, and books (Dumpert, and relies on the pick-up of bait particles by foraging workers and their 1981). This species is also able to chew on silk, rayon, rubber and transfers to other colony members (Jordan et al., 2013). Baits have been electrical wiring (Hölldobler and Wilson, 1990). In hospitals, the successfully used to control a number of social pests (Jordan Pharaoh ant is reputed to carry several pathogenic bacteria (Haack and et al., 2013). However, many bait-based programs are failed due to

⁎ Corresponding author at: Household and Structural Urban Entomology Laboratory, School of Biological Sciences, Universiti Sains Malaysia, Penang, Malaysia. E-mail address: abdhafi[email protected] (A.H. Ab Majid). https://doi.org/10.1016/j.aspen.2017.11.005 Received 26 January 2017; Received in revised form 23 October 2017; Accepted 6 November 2017 Available online 07 November 2017 1226-8615/ © 2017 Published by Elsevier B.V. on behalf of Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society. A.H. Ab Majid et al. Journal of Asia-Pacific Entomology 21 (2018) 46–51 insecticide resistance and insufficient level of attractiveness (Rust et al., adopted from Shirwaikar et al. (2004) in their efforts to prevent the 2002; Krushelnycky and Gillespie, 2008). Thus, the ability to produce escape of trapped workers. A minute amount of peanut butter or honey bait with high attractiveness remains a major challenge for the bait- held on a small piece of paper was placed inside all traps to serve as based ant control strategy. For target ants to pick up and transfer bait feed. After 3 h of collection, the trapped workers were kept in 250-mL particles to the colony, they must be attracted to the bait. Therefore, the plastic containers lined with Fluon coat and labeled according to spe- first and critical step in the bait use process is attracting the target ants, cies, colony number, and date of sampling. The workers' samples were particularly the foragers (Jordan et al., 2013). brought to the insectarium of the School of Biological Sciences (Uni- The sense of smell is one of the main sensory modalities for ants versiti Sains Malaysia). Subsamples were kept in 90% ethanol for spe- (Gronenberg, 2008; Choe et al., 2012). In fact, they primarily perceive cies identity confirmation. The laboratory conditions were the world through smell via the detection of airborne chemicals and 27 °C ± 2.0 °C, 75% ± 1% relative humidity (RH), in photoperiod touch (Gronenberg, 2008). Since the first line in the bait use process is 13:10 h (light:dark) with 1 h of dusk. Workers that had acclimatized to to entice foragers (Jordan et al., 2013) and those olfactory cues are the laboratory environment and were active after a 12 h-starvation essential for social organization and behaviors (Gronenberg, 2008), period, were used as experimental subjects. especially orientation (Wolf and Wehner, 2000), these aspects of ant biology should receive the highest attention when seeking new control Coffee materials and experimental extracts strategies. Despite substantial efforts to increase bait attractiveness by the addition of insect tissue (Williams et al., 1990), different fruit juices Local varieties of Coffea arabica (Arabica), C. canephora (Robusta) (Lucas and Invest, 1993), sugars, proteins, oils, or a combination of and C. liberica (Liberica) obtained from Cap Kuda Coffee Company, different attractants (Rust et al., 2002), only few available baits are Sabah were selected for this study. Coffee beans were roasted with no highly attractive to ants (Rust et al., 2002). Since odors can influence sugar compounds added. The temperatures ranged from 210 °C to the behavior of , it is, therefore, an important strategy to target 240 °C were used in the roasting process with the roasting time of 12 to strong-smelling and chemically rich materials to be used as baits. 30 min. Approximately, 150 g of dried and roasted coffee beans were Coffee is one of the promising candidates as it has over 800 aromatic individually crushed using a blender (Pensonic Blender PEN-PB3103; compounds (Clarke and Macrae, 2012). Many of these constituents such Senheng® Electric Sdn. Bhd., Kuala Lumpur, Malaysia) for 10 min. In as aliphatics—carbonyl and sulfur contain compounds: alicyclic ele- order to obtain uniform textures, grounds were sieved twice through a ments—ketones; aromatic benzenoid compounds—phenols; hetero- kitchen sieve strainer (250-wire mesh). Fine grounds were used to cyclic compounds—furans, hydrofurans, pyrroles, pyridines, quino- produce different extracts by Soxhlet extraction in accordance with the lines, pyrazines, quinoxalines, indoles, thiophens, thiophenones, published procedures (Cholakov et al., 2013). Briefly, an amount of thiazoles and oxazoles are produced during the roasting process (Illy 50 g of fine Arabica grounds was placed on a paper thimble and ex- and Illy, 2015; Fisk et al., 2012; Clarke and Macrae, 2012). The in- tracted with 250 mL of methanol. Five hours after the first down- creased diversity of compounds results in an aroma complex comprising pouring of the methanol from the thimble, the resulting mixture (me- fruity, earthy, catty, roasty, spicy, buttery, sweet, rotten cabbage-like, thanol + extract) was siphoned into a flat-bottomed flask, filtered and honey-like, potato-like, caramel-like, seasoning-like, and vanilla-like transferred into a glass petri dish. The extract was placed in an in- smells (Grosch, 1998). These smells hit many scent receptors in both cubator (Memmert GmbH + Co, KG, Germany) set at 20 °C. After humans and animals including > 900 species of insects as coffee pests. 3 days of evaporation, the extract (referred to as Arabica extract) was For instance, exposure of rats to coffee aroma deprived them of sleep for kept in a vial and stored in a freezer (−4 °C) until used. The same a day (Seo et al., 2008). In honey bees, caffeine from coffee stimulated quantity of fine grounds and procedures were also performed for Ro- responses in olfactory learning and memory (Wright et al., 2013). Many busta and Liberica grounds; of which the two resulting juices were processes inherent to social living and food processing in bees possess accordingly designated as Robusta and Liberica extracts. homologs in ants. As bees are genetically related to ants (Johnson et al., Another three experimental concentrations of coffee i.e. 0.01%, 2013) and have far more glomeruli than ants (160 glomeruli) (Flanagan 0.05% and 0.10% were produced using Arabica, following a slightly and Mercer, 1989), they may be highly responsive to the aroma of modified method of Derraik and Slaney (2005). To prepare 0.01% coffee. Despite evidence that coffee has a variety of aromas and that Arabica solution, an amount of 0.005 g of powdered roasted grounds caffeine influences some hymenopterans (bees), where hymenopterans was placed into a 150-mL glass cup with 50 mL of boiling water. After attracted to caffeine in flower nectar. However, there have been no 10 min, the resulting solution was sieved through a piece of fine-mesh studies on the effects of coffee on ant foraging behaviors with respect to mosquito net as in Satho et al. (2015). This solution was designated as bait technology improvement. The present study was carried out to “ONE”. Meanwhile, to prepare 0.05% and 0.10% solutions, the amounts examine the behavioral responses of household ants towards extracts of 0.025 g and 0.05 g of Arabica grounds were used following the same from different coffee species. The behaviors of these ants in response to procedures and were referred to as TWO (0.05%) and THREE (0.10%), coffee exposure at three different concentrations and sugar contents respectively. To acquire a sugared experimental Arabica, we proceeded were also probed. as follows. An amount 0.005 g of powdered roasted Arabica grounds was immersed in 50 mL of boiling water in a 150-mL glass cup and was Materials and methods allowed to disintegrate. After 10 min, the resulting solution was filtered and 0.25 g of coarse grain sugar (Gula Prai, MSM Holdings, Malaysia) Test ant species and experimental subjects was added. The solution was referred to as “S” (0.50% of sugar). An- other solution was prepared using the same procedures with no sugar T. indicum (TI), M. pharaonis (MP) and S. geminata (SG) were used in added and was referred to as “NS”. A volume of 50 mL cooled boiled this study. For each of these ant species, colonies were located within water was also prepared as a control (C). the Minden Campus of University of Science Malaysia (Penang, Malaysia, latitudes 5°8′N–5°3′N; longitudes 100°8′E–100°32′E). For Bioassays setup each of the three formicine ants, two different colonies were selected as sources of test subjects, and each was marked using tagged wooden A Y-tube olfactometer system previously described by Yusuf et al. stakes. Active workers were collected by placing twenty to thirty traps (2014) was used to test the attraction of workers of different household within each colony starting from 7 am. Each trap consisted of a 1.5-mL ant pests to odors emanating from di fferent coffee extracts. The system Eppendorf tube with the lower bottom removed and was interiorly comprised of a central tube (7.5 cm long) and two lateral arms (each lined with a thin layer of Fluon (Polytetrafluroethylene suspension), 5.75 cm long and 10 mm wide). Each arm was connected to a glass

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